In the United States, soybean sudden death syndrome is caused by the soil borne ascomycete Fusarium virguliforme. Recent studies revealed that F. virguliforme colonizes additional crop species, including corn; specifically, and with significance to our work, corn is an asymptomatic host of F. virguliforme. This asymptomatic interaction provides a unique application to uncover novel pathogen responses that are important for both endophytic and pathogenic processes on two different hosts. A comprehensive analysis of F. virguliforme transcriptomes from colonized soybean and corn over a 14-day time course uncovered a nearly complete network rewiring, with less than 8% average gene co-expression module overlap upon colonizing the different hosts. Fungal modules were uniquely enriched for catabolic processes of amino acids and sugars within soybean, yet co-expression clustering was enriched for upregulation of primary metabolism processes on corn. Differential gene expression highlighted a significant upregulation of carbohydrate-active enzymes on soybean when compared to corn as F. virguliforme shifted from biotrophic to necrotrophic lifestyle over 14 days. Interestingly, toxin production was similar upon both hosts. This analysis reveals the ability of a fungal pathogen on soybean to rewire a transcriptional program to asymptomatically colonize a corn, rotational crop of soybean, potentially enabling persistence in agroecosystems.